The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 86, Issue 8

Scientific Articles | August 01, 2004

Preoperative Marking of Musculoskeletal Tumors Guided by Magnetic Resonance Imaging

Philippe L. Pereira, MD¹; Jan Fritz¹; Claudius W. Koenig, MD¹; Franz Maurer, MD²; Paul Boehm, MD³; Andreas Badke, MD²; Markus Mueller-Schimpfle, MD¹; Michael Bitzer, MD¹; Claus D. Claussen, MD¹

¹ Department of Diagnostic Radiology, Eberhard-Karls-University, Hoppe-Seyler-Strasse 3, D-72076 Tuebingen, Germany. E-mail address for P.L. Pereira: philippe.pereira@med.uni-tuebingen.de
² Trauma Center, Eberhard-Karls-University, Hoppe-Seyler-Strasse 3, D-72076 Tuebingen, Germany
³ Department of Orthopedic Surgery, Eberhard-Karls-University, Hoppe-Seyler-Strasse 3, D-72076 Tuebingen, Germany

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The authors did not receive grants or outside funding in support of their research or preparation of this manuscript. They did not receive payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

Investigation performed at the Department of Diagnostic Radiology, Trauma Center, and Department of Orthopedic Surgery, Eberhard-Karls-University, Tuebingen, Germany

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J Bone Joint Surg Am, 2004 Aug 01;86(8):1761-1767

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Abstract

Background: The purpose of this study was to evaluate a new stereotactic method for preoperative coil-marking of musculoskeletal tumors with use of interventional magnetic resonance imaging.

Methods: Nine patients with a soft-tissue or bone-marrow tumor were referred to our department for preoperative marking of the extent of the lesion. In one patient, two lesions were marked. Guidance for the punctures and the delivery of the coils was provided by an open low-field magnetic resonance imaging system with horizontal access. After imaging of the extent of the lesion, magnetic resonance imaging-compatible titanium coils were placed with use of nearly real-time or step-by-step magnetic resonance imaging control. The coils were placed up to seventy-two hours before the surgery. The inclusion of the tumor borders within the area of the excision was examined with cross-sectional histological analysis of surgical specimens.

Results: The tumor-marking intervention was successfully performed with the guidance of magnetic resonance imaging only in all patients. Preoperatively, nineteen coils were used to mark the ten lesions in the nine patients. All of the coils were easily located with intraoperative fluoroscopy. No coil migrated between the time of the percutaneous marking and the surgery. Histological examination of the resection borders revealed no residual tumor cells. No complications were observed, and, after a mean of twenty-three months of follow-up, no tumor had recurred.

Conclusions: Preoperative coil-marking guided by magnetic resonance imaging for exact delineation of a musculoskeletal tumor is technically feasible and can readily demonstrate the full extent of the tumor. Use of magnetic resonance fluoroscopy reduces the time needed for the intervention. We recommend the coil-marking technique.

Level of Evidence: Diagnostic study, Level II-1 (development of diagnostic criteria on the basis of consecutive patients [with universally applied reference "gold" standard]). See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

Different methods for percutaneous tissue-marking have been developed to guide surgery and allow more precise and tissue-sparing resection of tumors. Marking with methylene blue or hook-wires under computer tomography guidance before lung surgery^1-3 or resection of small osteoid osteomas^4,5 has been widely reported. Additional guiding methods include application of radionuclides to detect bone lesions with abnormal metabolism⁶ or marking with ultrasound guidance⁷. Guidance with magnetic resonance imaging has proved useful in neurosurgery⁸ and, with insertion of curved wires⁹ or coils¹⁰, prior to breast surgery. It is necessary to mark tumor margins preoperatively because of the difficulties in defining the extent of the tumor with only macroscopic inspection or fluoroscopy during surgery. Imprecise localization of tumor tissue may result in either insufficient excision, with an increased risk of recurrence, or excessive removal of healthy tissue. In addition, repeated removal of tissue for frozen-section analysis can extend the duration of surgical intervention markedly and may result in a larger resection than necessary, with potentially increased morbidity.

Magnetic resonance imaging allows detection of multifocal soft-tissue and bone-marrow lesions with high sensitivity^11,12 and without radiation¹³. In addition, with the use of optimized magnetic resonance imaging sequences, contrast agents can be avoided during interventional procedures. The development of open magnetic resonance imaging units¹⁴ and of a new generation of flared closed units has dramatically expanded the possibilities in the field of interventional magnetic resonance imaging. With interactive, nearly real-time imaging, precise device control, and good access to patients, this technology is ideal for minimally invasive interventions^15,16.

The goal of this prospective study was to develop, and to evaluate the feasibility, safety, and efficacy of, stereotactic preoperative tumor-marking with use of a low-field open magnetic resonance imaging unit with a circular body coil for the exact delivery of a commercially available titanium coil.

Materials and Methods

Materials and Methods | Results | Discussion | Acknowledgements | References

Between July 2002 and May 2003, magnetic resonance imaging-guided marking of tumor margins was performed in nine patients (seven men and two women with an age range of twenty-six to eighty-one years and a median age of fifty-four years) who had a proven indication for surgical tumor resection. Seven patients had a soft-tissue tumor, and two had a bone-marrow tumor (Table I). One patient had two tumors. The patients were consecutively enrolled in the study. Written informed consent for use of medical records for research purposes and scientific publication was obtained from all patients. All patients were informed about the benefits and risks of the interventional marking procedure.

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TABLE I Clinical Data

Case	Age (yr)	Gender	Histopathological Diagnosis	Tumor Size (cm)	No. of Coils	Type of Lesion	Location of Lesion
1	65	M	Leiomyosarcoma	11.5 × 6 × 4.5	2	Soft tissue	Prox. part of lower limb
2	37	M	Neurinoma	1 × 0.5 × 1	2	Soft tissue	Dist. part of lower limb
3	38	M	Liposarcoma	9 × 2 × 2	2	Soft tissue	Dist. part of lower limb
4	66	M	Metastasis (renal cell carcinoma)	4.5 × 1.5 × 1.5	2	Bone marrow	Prox. part of lower limb
5	54	M	Metastasis (adenocarcinoma)	3 × 1.6 × 2	2	Bone marrow	Upper arm
6	77	F	Liposarcoma	5 × 4 × 3	2	Soft tissue	Pelvis
				0.5 × 0.5 × 1	1
7	26	M	Fibroma	8 × 1.7 × 2	2	Soft tissue	Dist. part of lower limb
8	81	M	Lymphoma	12 × 6 × 3	2	Soft tissue	Dist. part of lower limb
9	59	F	Fibrosarcoma	4 × 1.5 × 2	2	Soft tissue	Shoulder

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TABLE I Clinical Data

Case	Age (yr)	Gender	Histopathological Diagnosis	Tumor Size (cm)	No. of Coils	Type of Lesion	Location of Lesion
1	65	M	Leiomyosarcoma	11.5 × 6 × 4.5	2	Soft tissue	Prox. part of lower limb
2	37	M	Neurinoma	1 × 0.5 × 1	2	Soft tissue	Dist. part of lower limb
3	38	M	Liposarcoma	9 × 2 × 2	2	Soft tissue	Dist. part of lower limb
4	66	M	Metastasis (renal cell carcinoma)	4.5 × 1.5 × 1.5	2	Bone marrow	Prox. part of lower limb
5	54	M	Metastasis (adenocarcinoma)	3 × 1.6 × 2	2	Bone marrow	Upper arm
6	77	F	Liposarcoma	5 × 4 × 3	2	Soft tissue	Pelvis
				0.5 × 0.5 × 1	1
7	26	M	Fibroma	8 × 1.7 × 2	2	Soft tissue	Dist. part of lower limb
8	81	M	Lymphoma	12 × 6 × 3	2	Soft tissue	Dist. part of lower limb
9	59	F	Fibrosarcoma	4 × 1.5 × 2	2	Soft tissue	Shoulder

Study Design

All patients underwent a preinterventional high-field magnetic resonance imaging examination within the four weeks prior to the tumor-marking intervention. The decision regarding whether magnetic resonance imaging-guided tumor-marking was indicated was made by an interdisciplinary oncology board, and the marking was performed one to four weeks after the surgeon requested it. The surgical excision of the tumor was performed twenty-four to seventy-two hours after coil placement. In all cases, specimens were taken from the excision cavity to ensure, by means of histological analysis, that the remaining tissue was free of tumor cells. Inclusion criteria were a clinically occult musculoskeletal tumor or insufficient demarcation of the tumor by conventional imaging modalities. Exclusion criteria were ferromagnetic fragments or clips near to the central nervous system or to large vessels, ferromagnetic artificial heart valves, insulin pumps, and cochlear implants.

Magnetic Resonance Imaging Intervention

The entire intervention was performed with use of a 0.2-T c-shaped open magnetic resonance imaging unit (Magnetom Open; Siemens, Erlangen, Germany) with use of circular polarized, phased-array body coils (Siemens) with diameters ranging from 21 to 45 cm. A shielded free in-room magnetic resonance imaging monitor (Siemens) with a liquid-crystal display was used by the interventional radiologist for action control during magnetic resonance fluoroscopy.

Gadolinium-DTPA (Magnevist; Schering, Berlin, Germany) was administered (0.1 mmol/kg body weight) to the first two patients, whereas no contrast medium was necessary for the following seven patients. All lesions were marked with a coaxial 19.5 G magnetic resonance imaging-compatible titanium coil system (MReye, Cook Europe, Bjaeverskov, Denmark) (Fig. 1) that had been originally developed to mark small breast lesions¹⁰.

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Fig. 1: Coil-marking set (from top to bottom): the 19.5 G positioning needle with the trocar tip, the pusher, and the stopper and stylet with the titanium coil.

Tumors were visualized with a T2-weighted two-dimensional fast low-angle-shot (FLASH-2D) sequence (17-ms echo time, 30° flip angle, 6-mm slice thickness, and 96 × 256 matrix), a T1-weighted spin-echo sequence (15-ms echo time, 90° flip angle, 4 to 6-mm slice thickness, and 192 × 256 matrix), and a T2-weighted turbo spin-echo sequence (102-ms echo time, 90° flip angle, 6-mm slice thickness, and 168 × 256 matrix). To evaluate the puncture level and for needle guidance, nearly real-time magnetic resonance fluoroscopy¹⁷ with a fast-imaging steady-state precession (FISP) sequence (17.8-ms repetition time, 8.1-ms echo time, 90° flip angle, 8-mm slice thickness, 48 × 128 matrix, and 1-sec acquisition time) was used¹⁸. Nearly real-time imaging with magnetic resonance fluoroscopy was achieved by updating the magnetic resonance image approximately every 1.3 seconds. Alternatively, an axial FLASH-2D sequence (7.4-ms echo time, 70° flip angle, 6 to 8-mm slice thickness, and 96 × 256 matrix) was used to visualize the needle. Finally the coil position was visualized with an artifact-amplifying FLASH-2D sequence (40-ms echo time, 70° flip angle, 6-mm slice thickness, and 96 × 256 matrix).

Magnetic resonance imaging was performed to determine the sequence with the best contrast at low field. After precise evaluation of the entire extent of the tumor, a contrast medium-filled grid (TargoGrid; MRI Devices Daum, Schwerin, Germany) was placed above the region of interest. Cutaneous points superficial to the tumor were initially visualized with magnetic resonance fluoroscopy, with use of nifedipine (Adalat) pills as markers or the operator's finger as a marker. Following verification with the magnetic resonance imaging, the margins of the tumor were marked on the skin with ink. Before needle placement, the puncture site was prepared and draped in a sterile fashion. Lidocaine (Xylocaine, 2%) was instilled subcutaneously at the region of interest. For marking of soft-tissue tumors, coils were placed in normal tissue adjacent to the tumor borders. The coils were placed as close as possible to the tumor margins with strict avoidance of contact with the tumor to avoid the risk of tumor-cell seeding. To mark the bone-marrow tumors, coils were placed in adjacent tissue lying on the corresponding bone at the proximal and distal poles of the lesion, as visualized in the transverse axis (Fig. 2-A). In five patients (Cases 1 through 5), the needles were placed with step-by-step imaging with short FLASH-2D sequences. After FISP sequences became available, the patients (Cases 6 through 9) had the coils placed with the guidance of nearly real-time magnetic resonance fluoroscopy with in-room monitoring. After needle placement, two perpendicular control sequences were performed on the needle tip to ensure exact placement near the tumor border. The trocar of the positioning needle was then replaced by the preloaded stylet. On removal of the stylet, a stopper ensured that the coil was left in the positioning needle. Finally, the pusher was introduced into the needle to deliver the coil. A final magnetic resonance imaging sequence confirmed successful placement (Figs. 2-B, 2-C, and 3-B).

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Figs. 2-A through 2-D: Case 4. T1-weighted spin-echo sequence acquired during coil placement. After excision of the tumor, histopathological analysis disclosed a metastatic renal cell carcinoma in the bone marrow of the femur. Fig. 2-A Coronal image acquired after placement of both magnetic resonance imaging-compatible needles (arrows).

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Figs. 2-B and 2-C: Paraosseously delivered coils (arrows) at the upper (Fig. 2-B) and lower (Fig. 2-C) poles of the lesion producing a small artifact.

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Figs. 3-A and 3-B: Fig. 3-A Magnetic resonance fluoroscopy performed with an axial fast-imaging steady-state precession (FISP) sequence for evaluation of the puncture site. The arrow indicates the operator's finger during the fluoroscopy. Fig. 3-B Axial two-dimensional fast low-angle-shot (FLASH-2D) sequence after coil placement, demonstrating the needle (black arrow) and the delivered coil (white arrow).

After the magnetic resonance imaging intervention, radiographic imaging was performed for all patients according to a standard protocol (Fig. 2-D). Intraoperative fluoroscopic images were compared with these postinterventional radiographs to confirm that the positions of the coils had remained the same.

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Fig. 2-D: Postinterventional radiograph showing the delivered coils in a paraosseous location (arrows).

Results

Materials and Methods | Results | Discussion | Acknowledgements | References

To mark the ten tumors in the nine patients, nineteen coils were placed, all successfully. All but one of the lesions were marked with two coils under the guidance of magnetic resonance imaging. Two coil pairs were placed paraosseously, and seven coil pairs were placed in the surrounding normal tissue bordering the tumor area. In one patient (Case 6), a small "satellite lesion" was marked with an additional single coil (Table I). No complications occurred during or after coil placement. The magnetic resonance imaging intervention was well tolerated by all patients, and it did not interfere with or complicate the surgical resection in any patient. Comparison of the coil positions on the postinterventional radiographs with those evaluated with the intraoperative fluoroscopy demonstrated no evidence of coil migration. Contrast medium was used in our first two patients, but with the use of T2-weighted FLASH-2D sequences all lesions in the rest of the patients were sufficiently delineated without injection of contrast medium. The coils were easily identified with intraoperative fluoroscopy in all patients.

Biopsy specimens were taken from the cavity wall after excision of the tumors, and histopathological examination of those specimens demonstrated no residual tumor cells after any resection. A moderate granulomatous inflammatory reaction surrounding the coil was identified histologically in one patient who had undergone the surgery seventy-two hours after coil-marking.

Magnetic Resonance Imaging Intervention

The mean duration of the magnetic resonance imaging intervention, including the preinterventional and postinterventional care of the patient, was seventy-three minutes (range, fifty-two to 114 minutes). All interventions were performed by the same radiologist. Preinterventional and postinterventional imaging required a mean of thirty-eight minutes (range, twenty-seven to fifty-six minutes). Most of the procedure time was spent in preinterventional imaging and developing an adequate plan for coil placement, including patient positioning. The average preinterventional procedure time decreased from thirty-seven minutes (range, twenty-nine to forty-eight minutes) for the first five patients to twenty-two minutes (range, eighteen to twenty-six minutes) for the last four patients. The average time for coil placement decreased from ten minutes (range, seven to twenty-one minutes) for the first five patients to six minutes (range, four to nine minutes) for the last four patients. The overall decrease in the procedure time was due to a faster coil-placement strategy and a faster technique of coil placement with use of magnetic resonance fluoroscopy. The coils were placed one day before the surgery in five patients, two days before the surgery in three, and three days before the surgery in one.

Discussion

Materials and Methods | Results | Discussion | Acknowledgements | References

Marking with a coil system has advantages over other marking methods. Liquid markers have a tendency to distribute nonspecifically into the adjacent tissue¹⁹, and migration of hook-wires and curved-end wires has been reported^20-23. As the coils that we used are located within the tissue, without connection to the skin surface, they do not dislocate or displace⁹ or migrate. Furthermore, when lesions are marked with coils, a longer time between marking and surgery can be tolerated. In this study, patients underwent surgery up to three days after coil placement, without complications. The precise marking of the margins of the abnormal tissue improved preoperative planning, providing the surgeon with valuable information regarding the optimal incision and leading to a less invasive and more biologically sparing tumor excision as well as achieving macroscopically complete tumor resections.

With use of magnetic resonance imaging, it was possible to delineate abnormal and normal tissue more precisely. The FLASH-2D sequence proved to be feasible for evaluation of the puncture site and coil placement with the step-by-step method. The FLASH-2D sequence is characterized by good tissue contrast with high resolution (Fig. 3-B). However, because of the long acquisition times, FLASH-2D sequences are not feasible for magnetic resonance fluoroscopy. Magnetic resonance imaging with FISP sequences is characterized by lower resolution with a lower tissue contrast, but it provides fast imaging of a sufficient quality for evaluation of the puncture site and coil placement (Fig. 3-A). FISP sequences are feasible for magnetic resonance fluoroscopy because of their short acquisition times. In this study, magnetic resonance fluoroscopy in combination with use of an open magnetic resonance imaging unit and an in-room monitor proved to be an advantageous and time-saving way to evaluate the puncture site and coil placement. It provided nearly real-time action control and therefore more exact and faster device placement.

Clinical and radiographic follow-up as well as evaluation of a larger number of patients is needed to determine whether this method is worth the effort and cost. The recurrence rate after excision following tumor marking and the operative time have to be compared with the recurrence rate and surgical duration without preoperative tumor marking. Interventional magnetic resonance imaging provides an easy and safe way for exact marking of clinically occult tumors or tumors that are insufficiently demarcated with conventional imaging modalities. With increasing experience and the use of magnetic resonance fluoroscopy, the duration of the intervention can be reduced substantially. Because of the limited availability of the interventional equipment, this procedure is currently available only at specialized centers. However, the new flared closed magnetic resonance imaging scanners with a short, wide-bore magnet permit procedures such as those that we described to be performed without a special interventional magnetic resonance imaging suite.

Acknowledgements

Materials and Methods | Results | Discussion | Acknowledgements | References

Note: The authors thank Paul Edward Pfeffer, University College London, United Kingdom, for his assistance in the preparation of this manuscript.

References

Materials and Methods | Results | Discussion | Acknowledgements | References

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Topics

fluoroscopy ; neoplasms ; vibration ; neoplasm of musculoskeletal system

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Philippe L. Pereira, Jan Fritz, Claudius W. Koenig, Franz Maurer, Paul Boehm, Andreas Badke, Markus Mueller-Schimpfle, Michael Bitzer, Claus D. Claussen; Preoperative Marking of Musculoskeletal Tumors Guided by Magnetic Resonance Imaging. The Journal of Bone & Joint Surgery. 2004 Aug;86(8):1761-1767.

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